PCP signaling and ciliogenesis in vertebrate embryos

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Abstract

The vertebrate planar cell polarity (PCP) pathway has been previously found to control polarized cell behaviors rather than cell fate. We report here that disruption of Xenopus laevis orthologs of the Drosophila melanogaster PCP genes Xint or Xfy affected not only PCP-dependent convergent extension but also caused embryonic phenotypes consistent with defective Hedgehog signaling. These defects in Hedgehog signaling resulted from a broad requirement for Inturned and Fuzzy in ciliogenesis. We show that these proteins are necessary for the formation of both primary cilium in the neural tube and multi-cilia in the epidermis. Also, using Xenopus muco-ciliary epidermis, we demonstrated that one of the core PCP genes Dishevelled performs dual functions in ciliogenesis, basal body docking and planar polarization of ciliary beating. To this end, we showed that Dishevelled works in concert with the PCP effector protein Inturned and Rho GTPase to mediate the docking of basal bodies to the apical cell surface. We suggest that this docking involves a Dvl-dependent association of basal bodies with vesicles, and with the vesicle-trafficking protein Sec8. Finally, we showed that independent of their roles in apical docking, Dvl/PCP signaling is required again for directional ciliary beating. For the first time, this study uncovered the mechanism for controlling the apical docking of basal bodies. Moreover, the results suggest that the same Dvl/PCP signaling is also important for the planar polarization of ciliary beating in a vertebrate muco-ciliary epithelium.